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Gram-negative bacteria associated with a dominant arboreal ant species outcompete phyllosphere-associated bacteria species in a tropical canopy

  • Plant-microbe-animal interactions – original research
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Abstract

Ants have efficient and well-studied social immunity mechanisms, which prevent the colony contamination. Little is known about how workers keep their outside territory clear of diseases. We investigated the interactions between Azteca chartifex ants, their associated bacteria and bacteria on the phyllosphere of Byrsonima sericea trees, comparing plants patrolled and not by the ants. The hypothesis is that bacteria associated with the worker’s exoskeleton may outcompete the leaf bacteria. Culturable bacteria were isolated from ants, from the main and satellite nests, and from phyllosphere of B. sericea taken from trees that had A. chartifex nests and from trees without nests. The isolates were grouped by Gram guilds and identified at the genus level. There was a higher percentage of Gram-negative isolates in the ants and on the leaves patrolled by them. There was a higher growth rate of ant bacteria from the main nest compared to those found in ants from the satellite nests. The most representative genus among ant isolates was Enterobacter, also found on leaves patrolled by ants. Under favourable in vitro conditions, A. chartifex Gram-negative bacteria outcompete leaf bacteria by overgrowth, showing a greater competition capacity over the Gram-positive bacteria from leaves with no previous interaction with ants in the field. It was demonstrated that ants carry bacteria capable of outcompeting exogenous bacteria associated with their outside territory. The leaf microbiota of a patrolled tree could be shaped by the ant microbiota, suggesting that large ant colonies may have a key role in structuring canopy plant–microbe interactions.

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Data availability

The 16S amplicon sequences has been deposited on GenBank under BioProject ID PRJNA590751.

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Acknowledgements

We thank CAPES for granting scholarships. We also thank FAPEMIG, Universidade Federal de Ouro Preto (UFOP) and Programa de Pós-Graduação em Ecologia de Biomas Tropicais for logistical and financial support. We are grateful to Rio Doce State Park (PERD), and its employees for the structure provided during data collection. SPR is researcher granted by CNPq (306572-2019-2).

Funding

This project was supported by the Post-Graduate Program in Tropical Biomes Ecology, from the Federal University of Ouro Preto. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Authors and Affiliations

Authors

Contributions

MB, SR and LM conceived the study hypotheses and the experimental 16 design. MB, SR and VP performed the sampling, data analysis and interpretation. MB performed 17 the experiments. MB and SR wrote the original draft and reviewed the manuscript.

Corresponding author

Correspondence to M. R. Bitar.

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Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Additional information

Communicated by Corné Pieterse.

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Bitar, M.R., Pinto, V.D., Moreira, L.M. et al. Gram-negative bacteria associated with a dominant arboreal ant species outcompete phyllosphere-associated bacteria species in a tropical canopy. Oecologia 195, 959–970 (2021). https://doi.org/10.1007/s00442-021-04878-y

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  • DOI: https://doi.org/10.1007/s00442-021-04878-y

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